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Latin american journal of aquatic research

versión On-line ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.43 no.3 Valparaíso jul. 2015 

Research Article


Total mercury in female Pacific sharpnose sharks Rhizoprionodon longurio and their embryos

Mercurio total en hembras del tiburón bironche, Rhizoprionodon longurio y en sus embriones


Martín G. Frías-Espericueta1, Francia K.G. Zamora-Sarabia2, J. Fernando Márquez-Farías1, J. Isidro Osuna-López1, Jorge Ruelas-Inzunza3 & Domenico Voltolina4

1 Facultad de Ciencias del Mar, Universidad Autónoma de Sinaloa Paseo Claussen s/n, Mazatlán, Sinaloa, 82000, México
Programa de Posgrado en Recursos Acuáticos, Facultad de Ciencias del Mar Universidad Autónoma de Sinaloa, Av. de los Deportes s/n, Ciudad Universitaria Mazatlán, Sinaloa 82017, México
Instituto Tecnológico de Mazatlán, Calle Corsario I N° 203, Col Urias
Mazatlán, Sinaloa 82070, México
Laboratorio de Estudios Ambientales UAS-CIBNOR, P.O. Box 1132 Mazatlán, Sinaloa 82000 México
Corresponding author: Domenico Voltolina (
Corresponding editor: Ricardo Prego

ABSTRACT. We determined the Hg content of blood, placenta and umbilical cord of 20 pregnant females of the viviparous Pacific sharpnose shark, Rhizoprionodon longurio and of the livers of the embryos contained in their right and left uterus, aiming to provide information on the amount of this metal offloaded during pregnancy by the mother to the embryos. Hg content varied by close or higher than one order of magnitude in all tissues and showed the decreasing trend: maternal blood > umbilical cord > placenta > embryonic livers, with placenta and embryonic livers significantly lower than maternal blood. There were highly significant correlations (P < 0.001) between the Hg content of maternal blood, cord, and placenta. Those between embryonic livers and maternal blood, cord and placenta were not significant (P > 0.05). The results suggest transplacental Hg transfer and that the liver is not the main site of Hg accumulation.

Keywords: mercury, maternal offloading, shark embryos, blood, placenta, umbilical cord.

RESUMEN. En el presente estudio se determinó el contenido de mercurio en la sangre, placenta y cordón umbilical de 20 hembras del tiburón bironche Rhizoprionodon longurio así como en el hígado de los embriones de los úteros derecho e izquierdo, con el objetivo de proveer información sobre la cantidad de este metal transferida por la madre a sus embriones durante su desarrollo. Los contenidos de Hg variaron hasta un orden de magnitud en todos los tejidos y presentaron el siguiente orden decreciente: sangre materna > cordón umbilical > placenta > hígado de los embriones. Los contenidos de la placenta y el hígado de los embriones fueron significativamente menores al determinado en la sangre materna. Se encontraron correlaciones altamente significativas (P < 0,001) entre el contenido de Hg de la sangre materna, cordón y placenta, mientras que las calculadas entre hígado de los embriones y la sangre materna, cordón y placenta no fueron significativas (P > 0,05). Los resultados sugieren que existe una libre transferencia de Hg y que el hígado no es el sitio principal de acumulación de Hg.

Palabras clave: mercurio, transferencia materna, embriones de tiburones, sangre, placenta, cordón umbilical.



Atmospheric transport and deposition are considered the main sources of Hg pollution, although industrial and urban wastes, mining, and agriculture are other important sources of Hg contamination of the aquatic environment (Harris et al., 2012). This has a high environmental cost, because it entails lower availability of recreational areas, loss of biodiversity and of access to natural food products for human consumption, and adverse health effects (Bellanger et al., 2013).

Along the food web, Hg excretion is generally lower than its absorption, and because of its progressive accumulation, this metal may reach high concentrations in the tissues of top predators (McMeans et al., 2015). This may explain the levels of Hg close or above the precautionary limits for human consumption detected in Mexican Pacific sharks (Escobar-Sánchez et al., 2011; Hurtado-Banda et al., 2012). This is a source of concern for human health and for the conservation of these species, because the pregnant mothers of viviparous sharks transfer to their embryos the toxic substances accumulated in their organs and tissues (Lyons & Lowe, 2013; Mull et al., 2013; Olin et al., 2014).

In mammals, maternal blood supplies oxygen and nutrients to developing embryos, but it is also the source of their exposure to contaminants (Leino et al., 2013) since, although the placenta may act as at least a partial barrier against Cd (Gundacker & Hengstschläger, 2012), Pb and Hg can readily cross this barrier (Gupta, 2012). Some results seem to show that embryos concentrate maternal blood-borne Hg, suggesting that they act a route of discharge of the excessive load of maternal mercury (Rudge et al., 2009).

In placental sharks, yolk sac and stalk become progressively modified into placenta and umbilical cord, with gas exchange and hematrophic functions similar to those of mammals. These shared basic maternal-fetal relationships seem to indicate convergent evolution of the two groups (Haines et al., 2006), with possible shared aspects of other functions of this organ such as acting as transport site or as partial barrier to some metals.

An important component of the winter landings of the artisanal fishing fleets of the Mexican Pacific NW is the sharpnose shark Rhizoprionodon longurio, which is a highly migratory placental viviparous species (Corro-Espinosa et al., 2011). In this work, we evaluated the Hg content of blood and placenta of pregnant R. longurio females and of the liver of their respective embryos, to provide information on the mother to embryo transfer of Hg in this species, which might be an important mechanism of impaired reproductive success.


Pregnant sharpnose sharks (20), obtained between January and March 2012 from local fishermen of Mazatlán (SE Gulf of California), were measured (total length, TL), and dissected in the laboratory with a stainless steel knife to obtain placenta and umbilical cord from the females and the liver of the embryos of both uteri. Blood (30 mL) was drawn from the ventral portion of females (Cizdziel et al., 2003) using sterile plastic syringes, and immediately placed in polyethylene tubes. All tissues were lyophilized for 72 h and homogenized in a Teflon mortar. Three samples of each tissue were digested at 130°C in a mod-block unit, using sealed Teflon vessels with 5 mL of concentrated HNO3 (trace metal grade). After digestion, samples were transferred to vials and diluted to 15 mL with Milli-Q water (Frías-Espericueta et al., 2014).

All materials used during sampling and metal analysis were acid washed. Total Hg was determined by cold vapor atomic absorption spectrophotometry (CV-AAS) after reduction with SnCl2 in a mercury analyzer (Buck Scientific). Certified reference material (DORM 3, National Research Council Canada) was used to assess the accuracy of the method, with a recovery of 105%, and blanks were included using the same procedure of the samples to check possible contamination. The limit of detection was 0.01 μg g-1 and the coefficient of variation was <10%.

The non-compliance with parametric assumptions led to employment of Mann-Whitney's tests to compare the mean Hg content of the livers of the embryos of the two uteri of each female. Since no significant differences were detected between uteri, the mean Hg content of the livers of all embryos obtained from each female was used for statistical comparisons between tissues, using non-parametric block ANOVA (Friedman's) and Dunn's multiple comparison tests. Possible relations between the Hg values found in the tissues of mothers and embryos were determined with Spearman's correlations tests. (ρ). All tests were with α = 0.05 (Zar, 1999).


Each female, with TLs ranging from 99.8 to 118.1 cm (mean 107.5 ± 4.9 cm), carried 4 to 11 embryos. The total number of embryos obtained from the 20 females was 168. Their TLs varied between 26.38 and 34.25 cm, and there was no significant difference in mean size between the mean values of right and left uterus-borne embryos (29.46 ± 2.53 and 29.75 ± 2.52 cm, respectively).

The Hg concentrations ranged between 0.16 and 1.97 μg g-1 dry weight in maternal blood and from 0.10 to 0.72 and 0.06 to 0.71 μg g-1 in cord and placenta, respectively. The mean values were 0.54 ± 0.52, 0.32 ± 0.17 and 0.20 ± 0.15 μg g-1, with a significant difference (P < 0.05) between blood and placenta, but not between blood and cord (Table 1). In embryonic livers total Hg ranged from 0.02 ± 0.01 to 0.16 ± 0.08 (right uterus) and between 0.04 ± 0.03 and 0.14 ± 0.02 μg g-1 (left uterus), and their global mean value was significantly lower than those of blood and cord, but not of the mean content of the placenta (Table 1).


Table 1. Mean Hg concentrations in μg/g, dw (± standard error) in blood,
cord and placenta of 20 pregnant Rhizoprionodon longurio and of the livers
of the respective embryos of the right (RU) and of the left (LU) uterus.

*Total mean values of blood, cord, placenta and embryonic livers ± standard
deviations. Equal or common letters indicate lack of significant differences
(Friedman's and Dunn's tests, α = 0.05; cd≤c≤bc≤ab and d<a).


There were significant correlations between the Hg content of blood and placenta (ρ = 0.943), blood and cord (ρ = 0.847), and between cord and placenta (ρ = 0.778), but the mercury contents of embryonic livers were not significantly related (P > 0.05) to the respective female tissues (Table 2). Additionally, there was no significant correlation between the Hg content of the embryonic livers with size and weight of the embryos (ρ = 0.005 and -0.1308, respectively, P > 0.05 in both cases) nor between total length of females with the respective blood Hg content (ρ = 0.231, P > 0.05).


Table 2. Spearman's correlation
coefficients (ρ) between the Hg contents
of tissues of females and embryos.



The greatest maternal offloading of contaminant occurs during the first reproductive event, when the loads of contaminants accumulated by the mother are at their highest values (Lyons & Lowe, 2013). The mean TL of the pregnant mothers indicates ages close to 8-10 years, and the smallest was 99.8 cm, which is reached at 4 to 5 years of age (Castillo et al., 1996). This indicates that none was primiparous, since the mean size at first maturity of this species is close to 93 cm (Corro-Espinosa et al., 2011).

Several authors found a significant relation between the Hg content of fish species and their TL, age or weight (Adams et al., 1999; Farkas et al., 2001). This does not correspond to our results, possibly because of the low variability in size of our specimens, as well as the fairly wide range of blood Hg concentrations. On the other hand, the good correlations between Hg contents of blood, cord and placenta coincide with the general agreement that blood Hg concentration is strongly related to the Hg content of the remaining tissues (Cizdziel et al., 2003; Schmitt & Brumbaugh, 2007). Among its several functions, blood distributes the products of digestion to all body tissues and carries metabolic wastes to the organs in charge of their excretion. This relation has been described also in humans (Ask et al., 2002; Rudge et al., 2009), although in these cases the Hg contents of cord or placental blood were higher than that of maternal blood.

The similar Hg contents of the embryonic livers obtained in right and left uterus confirm the lack of inter-uterine difference determined in other sharks by Adams et al. (1999), which was postulated by Frías-Espericueta et al. (2014) for other metals in the case of this species.

The sequence of progressively decreasing mean Hg concentrations of blood, cord, placenta and the lack of a significant difference between placenta and embryonic livers might indicate that the placenta acts as a partial barrier to transfer of toxic substances from mother to embryos. It also shows the existence of transplacental Hg transfer, possibly due to molecular mimicry with methionine of MeHg bound to thiol-groups (Ballatori, 2002). The content of the cord, intermediate between maternal blood and placenta, might therefore be due to the Hg fraction carried by maternal blood but not retained by the embryos, and possibly enriched by the embryos unloading their excess Hg to the mother.

There are many examples of higher Hg concentrations in fish liver tissues (Romeo et al., 1999; Mieiro et al., 2009; Guilherme et al., 2010; Azevedo et al., 2012), but a lower Hg liver content was observed in several fish species including sharks (Cizdziel et al., 2003; Kenšová et al., 2010; Lyons & Lowe, 2013). This difference coincides with the results obtained by Pethybridge et al. (2010) and Le Bourg et al. (2014) in embryos of placental and aplacental sharks, and is probably due to a lower content of inorganic than organic Hg, which has a high degree of affinity for the thiol groups of the muscle tissues (Soares et al., 2011).

In placental viviparous sharks, mercury transfer from mother to embryos is considered a detoxification mechanism of the mother (Adams et al., 1999), similar to the maternal offloading of organic pollutants described by Mull et al. (2013) and Olin et al. (2014) in the white shark Carcharodon carcharías and the bull shark, Carcharhinus leucas, respectively. Our results confirm that the placenta of the Pacific sharpnose shark Rhizoprionodon longurio is not an effective barrier to Hg transfer, which might be of concern because Hg might affect the normal embryonic development. This should be the focus of future studies concerning this, as well as other viviparous shark species.


Supported by PROFAPI 2011/060, PROMEP 103.5/ 13/9354 and CONACYT INFRA-2012-01-188029 grants. C. Ramírez helped in bibliographic search and C. Monroy in sampling.



Adams, D.H., J.R. McMichael & H. Robert. 1999. Mercury levels in four species of sharks from the Atlantic coast of Florida. Fish. Bull., 97: 372-379.         [ Links ]

Ask, K., A. Åkesson, M. Berglund & M. Vahter. 2002. Inorganic mercury and methylmercury in placentas of Swedish women. Environ. Health Persp., 110: 523-526.         [ Links ]

Azevedo, J.S., J.E. de Souza-Sarkis, T.A. Oliveira & T. Ulrich. 2012. Tissue-specific mercury concentrations in two catfish species from the Brazilian coast. Braz. J. Oceanogr., 60: 211-219.         [ Links ]

Ballatori, N. 2002. Transport of toxic metals by molecular mimicry. Environ. Health Persp., 110: 696-694.         [ Links ]

Bellanger, M., C. Pichery, D. Aerts, M. Berglund, A. Castaño, M. Čejchanová, P. Crettaz, F. Davidson, M. Esteban, M.E. Fischer, A.E. Gurzau, K. Halzlova, A. Katsonouri, L.E. Knudsen, M. Kolossa-Gehring, G. Koppen, D. Ligocka, A. Miklavcic, M.F. Reis, P. Rudnai, J.S. Tratnik, P. Weihe, E. Budtz-Jørgensen & P. Grandjean. 2013. Economic benefits of methyl-mercury exposure control in Europe: monetary value of neurotoxicity prevention. Environ. Health, 12: 3 doi: 10.1186/1476-069X-12-3.         [ Links ]

Castillo, L., F. Márquez, J. Uribe, R. Bonfil, D. De Anda, R. Vélez & D.O. Mendizábal. 1996. La pesquería de tiburón en México. In: Pesquerías relevantes de México, Instituto Nacional de Pesca, México, pp. 365-415.         [ Links ]

Cizdziel, J., T. Hinners, C. Cross & J. Pollard. 2003. Distribution of mercury in the tissues of five species of freshwater fish from Lake Mead, USA. J. Environ. Monit., 5: 802-807.         [ Links ]

Corro-Espinosa, D., J.F. Márquez-Farías & A. Muhlia-Melo. 2011. Size at maturity of the Pacific sharpnose shark Rhizoprionodon longurio in the Gulf of California, Mexico. Cienc. Mar., 37: 201-214.         [ Links ]

Escobar-Sánchez, O., F. Galván-Magaña & R. Rosíles-Martínez. 2011. Biomagnification of mercury and selenium in blue shark Prionace glauca from the Pacific Ocean off Mexico. Biol. Trace Element Res., 144: 550-559.         [ Links ]

Farkas, A., J. Salánki, A. Specziár & I. Varanka. 2001. Metal pollution as health indicator of lake ecosystems. Int. J. Occupat. Med. Environ. Health, 14: 163-170.         [ Links ]

Frías-Espericueta, M.G., N.G. Cárdenas-Nava, J.F. Márquez-Farías, J.I. Osuna-López, M.D. Muy-Rangel, W. Rubio-Carrasco & D. Voltolina. 2014. Cadmium, copper, lead, and zinc concentrations in female and embryonic Pacific sharpnose shark (Rhizoprionodon longurio) tissues. Bull. Environ. Contam. Toxicol., 93: 532-535.         [ Links ]

Guilherme, S., M.E. Pereira, M.A. Santos & M. Pacheco. 2010. Mercury distribution in key tissues of caged fish (Liza aurata) along an environmental mercury contamination gradient. In: N. Hamamura, S. Suzuki, S. Mendo, C.M. Barroso, H. Iwata & S. Tanabe (eds.). Interdisciplinary studies on environmental chemistry-biological responses to contaminants. Terrapub, Tokio, pp. 165-173.         [ Links ]

Gundacker, C. & M. Hengstschläger. 2012. The role of the placenta in fetal exposure to heavy metals. Wien Med. Wochenschr., 162: 201-206.         [ Links ]

Gupta, R.C. 2012. Veterinary toxicology. Basic and clinical principles, Academic Press, Waltham, 1250 pp.         [ Links ]

Haines, A.N., M.F. Flajnik & J.P. Wourms. 2006. Histology and immunology of the placenta in the atlantic sharpnose shark, Rhizoprionodon terraenovae. Placenta, 27: 1114-1123.         [ Links ]

Harris, R., C. Pollman, W. Landing, D. Evans, D. Axelrad, D. Hutchinson, S.L. Morey, D. Rumbold, D. Dukhovskoy, D.H. Adams, K. Vijayaraghavan, C. Holmes, R.D. Atkinson, T. Myers & E. Sunderland. 2012. Mercury in the Gulf of Mexico: sources to receptors. Environ. Res., 119: 42-52.         [ Links ]

Hurtado-Banda, R., A. Gomez-Alvarez, J.F. Márquez-Farías, M. Cordoba-Figueroa, G. Navarro-García & L.A. Medina-Juárez. 2012. Total mercury in liver and muscle tissue of two coastal sharks from the Northwest of Mexico. Bull. Environ. Contam. Toxicol., 88: 971-975.         [ Links ]

Kenšová, R., O. Čelechovská, J. Doubravová & Z. Svobodová. 2010. Concentrations of metals in tissues of fish from the Vëstonice reservoir. Acta Vet. Brno, 79: 335-345.

Le Bourg, B., J. Kiszka & P. Bustamante. 2014. Mother-embryo isotope (δ15N, δ13C) fractionation and mercury (Hg) transfer in aplacental deep-sea sharks. J. Fish Biol., 84: 1574-1581.

Leino, O., H. Kiviranta, A.K. Karjalainen, C. Kronberg-Kippila, H. Sinkko, E.H. Larsen, S. Virtanen & J.T. Tuomisto. 2013. Pollutant concentrations in placenta. Food Chem. Toxicol., 54: 59-69.         [ Links ]

Lyons, K. & C.G. Lowe. 2013. Mechanisms of maternal transfer of organochlorine contaminants and mercury in the common thresher shark (Alopias vulpinus). Can. J. Fish. Aquat. Sci., 70: 1667-1672.         [ Links ]

McMeans, B.C., M.T. Arts & A.T. Fisk. 2015. Impacts of food web structure and feeding behavior on mercury exposure in Greenland sharks (Somniosus micro-cephalus). Sci. Total Environ., 509-510: 216-225. doi:10.1016/j.scitotenv.2014.01.128.         [ Links ]

Mieiro, C.L., M. Pacheco, M.E. Pereira & A. Costa-Duarte. 2009. Mercury distribution in key tissues of fish (Liza aurata) inhabiting a contaminated estuary-implications for human and ecosystem health risk assessment. J. Environ. Monit., 11: 1004-1012.         [ Links ]

Mull, C.G., K. Lyons, M.E. Blasius, C. Winkler, J.B. O'Sullivan & C.G. Lowe. 2013. Evidence of maternal offloading of organic contaminants in white sharks (Carcharodon carcharias). PloS One, 8: 1-8.         [ Links ]

Olin, J.A., M. Beaudry, A.T. Fisk & G. Paterson. 2014. Age-related polychlorinated biphenyl dynamics in immature bull sharks (Carcharhinus leucas). Environ. Toxicol. Chem., 33: 35-43.         [ Links ]

Pethybridge, H., D. Cossa & E.C.V. Butler. 2010. Mercury in 16 demersal sharks from southeast Australia: biotic and abiotic sources of variation and consumer health implications. Mar. Environ. Res., 69: 18-26.         [ Links ]

Romeo, M., Y. Siau, Z. Sidoumou & M. Gnassia-Barelli. 1999. Heavy metal distribution in different fish species from the Mauritania coast. Sci. Total Environ., 232: 169-175.         [ Links ]

Rudge, C.V., H.B. Röllin, C.M. Nogueira, Y. Thomassen, M. Rudge & J.Ø. Odland. 2009. The placenta as a barrier for toxic and essential elements in paired maternal and cord blood samples of South African delivering women. J. Environ. Monit., 11: 1322-1330.         [ Links ]

Schmitt, C.J. & W.G. Brumbaugh. 2007. Evaluation of potentially nonlethal sampling methods for monitoring mercury concentrations in smallmouth bass (Micropterus dolomieu). Arch. Environ. Contam. Toxicol., 53: 84-95.         [ Links ]

Soares, T.M., D.A. Coutinho, L.D. Lacerda, M.O. Moraes & M.F. Rebelo. 2011. Mercury accumulation and metallothionein expression from aquafeeds by Litopenaeus vannamei Boone, 1931 under intensive aquaculture conditions. Braz. J. Biol., 71: 131-137.         [ Links ]

Zar, J.H. 1999. Biostatistical analysis. Prentice Hall, Upper Saddle River, 663 pp.         [ Links ]


Received: 30 October 2014;
Accepted: 17 February 2015


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